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Avian Blood Flukes (Digenea: Schistosomatidae) in North Dakota Susana Rios

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Avian Blood Flukes (Digenea: Schistosomatidae) in North Dakota Susana Rios University of North Dakota UND Scholarly Commons Theses and Dissertations Theses, Dissertations, and Senior Projects January 2014 Avian Blood Flukes (Digenea: Schistosomatidae) In North Dakota Susana Rios Follow this and additional works at: https://commons.und.edu/theses Recommended Citation Rios, Susana, "Avian Blood Flukes (Digenea: Schistosomatidae) In North Dakota" (2014). Theses and Dissertations. 1701. https://commons.und.edu/theses/1701 This Thesis is brought to you for free and open access by the Theses, Dissertations, and Senior Projects at UND Scholarly Commons. It has been accepted for inclusion in Theses and Dissertations by an authorized administrator of UND Scholarly Commons. For more information, please contact [email protected]. AVIAN BLOOD FLUKES (DIGENEA: SCHISTOSOMATIDAE) IN NORTH DAKOTA by Susana Rios Associate of Science, Johnson College, 2008 Bachelor of Science, Shippensburg University, 2012 A Thesis Submitted to the Graduate Faculty of the University of North Dakota in partial fulfillment of the requirements for the degree of Master of Science Grand Forks, North Dakota December 2014 Copyright 2014 Susana Rios ii iii PERMISSION Title Avian Blood Flukes (Digenea: Schistosomatidae) in North Dakota Department Biology Degree Master of Science In presenting this thesis in partial fulfillment of the requirements for a graduate degree from the University of North Dakota, I agree that the library of this University shall make it freely available for inspection. I further agree that permission for extensive copying for scholarly purposes may be granted by the professor who supervised my thesis work or, in his absence, by the Chairperson of the department or the dean of the School of Graduate Studies. It is understood that any copying or publication or other use of this thesis or part thereof for financial gain shall not be allowed without my written permission. It is also understood that due recognition shall be given to me and to the University of North Dakota in any scholarly use which may be made of any material in my thesis. Susana Rios December 1, 2014 iv TABLE OF CONTENTS LIST OF FIGURES…………………………………………………..…………………………viii LIST OF TABLES………………………………………………………………...…..…...……...x ACKNOWLEDGMENTS………………………………………………………………....….…xii ABSTRACT………………………………………………………………………………….…xiii CHAPTER I. INTRODUCTION………………………………………………………….……..1 Evolution and Phylogeny………………………………………………….2 Morphology…………………………………………………………......…4 Life Cycle………………………………………………………………….7 Snail Hosts…...………………………………………………..…..….….11 Avian Hosts…...………………………………………………………….11 Avian Health Concerns..……………………………………….……...…12 Effects of Avian Schistosomes in Humans and Other Mammals………………………………………………………..…….….14 Factors Influencing Avian Schistosomatid Diversity and Distribution………...………………………………………………..…...15 Current Status of Avian Schistosomatid Research in the United States……………………………………………………………….…….15 North Dakota as an Ideal Region to Study Avian Schistosomatids……………………………………………………...…..16 Research Objectives………...…………………...…………………...…..17 v II. METHODS AND MATERIALS………...……………………………...….……18 Snail Collection……..………………….…………………………..…….18 Snail Husbandry………………………...………………………..…..…..20 Cercarial Screening in Snails…...……………………………….…….…20 Bird Collection…...………………………………………….……..….…22 Bird Dissection Protocol…………...……………………………..….…..22 DNA Extraction…...…………………………………….………...……..23 Polymerase Chain Reaction……………………………………..……….24 DNA Sequencing………...………………………………………………30 Sequence Editing and Alignment…...………………………….…….…..30 Cercarial Morphology…………………………………….…….….…….31 Adult Fluke Morphology……..……………………….………..……..…31 Phylogenetic Analysis……...……………………………….……….…...32 Spatial and Occupancy Analysis of 2013 Snail Data……….............……33 III. RESULTS……………………………………………………………………..…34 Collected Snails and Avian Schistosomatid Prevalence…….………...…34 Cercariae: Species Identification and Host Associations…..…….….…...40 Adult flukes: Species Identification and Host Associations………....…..42 The Identification of Avian Schistosomatid Species by DNA Sequencing……...…………………………………………..……..…..…45 Intraspecific and Interspecific/Intergeneric Nucleotide Sequence Variation among Collected Avian Schistosomatids………...…...….…..45 Cercarial Morphology…………………………………………..…..……49 vi Adult Fluke Morphology…..…………………………………….………52 SEM Study of Trichobilharzia spp.………..…………………………………58 Phylogenetic Analysis…...…………………………………………...…..61 Spatial and Occupancy Analysis of 2013 Snail Data……….…………....70 IV. DISCUSSION……………………………………….…………………...………75 Intermediate Snail Hosts……..…………………………………………..75 Definitive Bird Hosts…..…………………………………………….…..78 Sequence Comparison and Phylogenetic Study of Avian Schistosomatids Found in North Dakota…………..…………………….80 Phylogenetic Interrelationships among Avian Schistosomatid Genera…...……………………………………………………………….81 Trichobilharzia……………………………………………….……….….82 Dendritobilharzia……………………………………………….………..83 Austrobilharzia……………………………………………………….….84 Gigantobilharzia……………………………………………...………….84 Cercarial Morphology……………………………………………...…….85 Cercarial Dermatitis in North Dakota……...……………………...……..85 APPENDICES……………………………………………………………………………...……87 A. Map of North Dakota Snail Collection Sites……..………………………..…….88 B. Recorded Data for all Snail Collection Sites…….………………………...…….89 C. Data on Snails Infected with Schistosomatidae Cercariae……..………………...93 REFERENCES………………………………………………………………………………..…97 vii LIST OF FIGURES Figure Page 1. Phylogenetic tree of Schistosomatidae based on Bayesian analysis of nuclear 28s rDNA (1200bp)……………...……………………………………………………..…3 2. Male and female avian schistosomatid, Ornithobilharzia sp……………………………...5 3. Variation in size and dimorphism between Schistosomatidae genera (Loker and Brant 2006)……….…………………………………………………..……………….6 4. Life cycle of avian schistosomatids…………………………………………………….....8 5. Phylogeny of intermediate snail hosts and their associated schistosomatidae parasites………………………………………………………………………..…………10 6. Representation of the sampling design used for snail collection. …………………….....19 7. Larval cercarial stage of an avian schistosomatid with identifying morphological features……………………………………………………………………………...……21 8. Ribosomal ITS and 28s nuclear regions showing positions of PCR and sequencing primers………….……………………………………………………….…..26 9. Positions of PCR and sequencing primers in the cox1 mitochondrial gene….………….27 10. All North Dakota snail collection sites from 2013 and the time (month) sites were visited and sampled…………………………………………………………..….…35 11. Map of North Dakota showing 2013 collection sites where AS infected snails were found……………………………………….……..………………………...36 12. Distribution of avian schistosomatid infected Stagnicola snails in North Dakota……………………………………………………...…………………………….37 13. Distribution of avian schistosomatid infected Lymnaea snails in North Dakota……………………………………………………………………………………38 viii 14. Distribution of avian schistosomatid infected Aplexa snails in North Dakota..........……39 15. Schistosomatidae species found within each snail genus and their prevalence……….…41 16. Morphology of a female Austrobilharzia sp. collected from an Avocet in North Dakota…………………………………………………………………..…………53 17. Morphological comparison between Dendritobilharzia sp. 1 and Dendritobilharzia sp. 2 adult female worms…………………………………………….54 18. Morphological comparison between Dendritobilharzia sp. 1 and Dendritobilharzia sp. 2 adult male worms………………………………………..……..55 19. Complete male Trichobilharzia specimen…………………………………………...…..56 20. Male Trichobilharzia sp. showing the genital opening, testes and terminal end of adult…...………………………………………………………………………….…...57 21. SEM images of a Trichobilharzia szidati cercaria……………………………………….59 22. SEM images of a Trichobilharzia querquedulae adult worm…………………...………60 23. Nuclear 28s rDNA Bayesian tree showing interrelationships among genera of the Schistosomatidae……………………………..…………………………………..…..62 24. A fragment of 28s rDNA Bayesian tree from Fig. 22 showing interrelationships among derived genera of Trichobilharzia, Allobilharzia and Anserobilharzia……….…63 25. Nuclear 28s rDNA Maximum Likelihood tree showing interrelationships among genera of the Schistosomatidae…………………………………………………….…….64 26. A fragment of the 28s rDNA Maximum Likelihood tree from Fig. 24 showing interrelationships among derived genera Trichobilharzia, Allobilharzia and Anserobilharzia……………………………………………………………………..……65 27. Nuclear 28s rDNA Bayesian tree of the derived avian schistosomatid clade…………....66 28. Mitochondrial cox1 Bayesian tree of the genus Trichobilharzia…………………….…..68 29. Mitochondrial cox1 Bayesian tree of Dendritobilharzia specimens collected in North Dakota and one sequence from GenBank……………………………….……..….69 30. Map of North Dakota showing all sites (numbered) where Schistosomatidae infected snails were collected ….……………………………………………..………....88 ix LIST OF TABLES Table Page 1. Thermocycling conditions for PCR amplification of 28s rDNA of avian schistosomatid cercariae and adult worms………………………………...……………..28 2. Thermocycling conditions for PCR amplification of mitochondrial cox1 mDNA of avian schistosomatid cercariae and adult worms……………….....…...……..28 3. PCR and sequencing primers for nuclear 28s and mitochondrial cox1 genes used in the study…………………………………………..……………………….……..29 4. Thermocycling conditions for sequencing reactions of nuclear 28s and mitochondrial cox1 DNA for all avian shcistosomatid cercariae and adult worms.….....30 5. Snail genera collected from North Dakota between May-September of 2013 and the number infected
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